Diabetic nephropathy: Protective factors and a new therapeutic paradigm

Journal of Diabetes and its Complications

Volumn 27, Issue 5, 2013, Pages 526-530

  Mima, Akira ^a  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

Author keywords

Angiopoietins; Diabetic nephropathy (DN); Dipeptidyl peptidase 4 (DPP 4) inhibitors; Endostatin; Glucagon like peptide 1 (GLP 1); Insulin Insulin receptor substrate 1 (IRS1); Protein kinase C (PKC); Src homology 2 domain containing phosphatase 1 (SHP 1); Tumstatin; Vascular endothelial growth factor (VEGF)

Indexed keywords

ACTIVATED PROTEIN C; ADIPONECTIN; ANGIOPOIETIN 1; CASPASE 8; DIPEPTIDYL PEPTIDASE IV INHIBITOR; ENDOSTATIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUCAGON LIKE PEPTIDE 1; HEME OXYGENASE 1; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INSULIN; INSULIN RECEPTOR; INSULIN RECEPTOR SUBSTRATE; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE; PHORBOL 13 ACETATE 12 MYRISTATE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN KINASE C; TUMOR NECROSIS FACTOR ALPHA; TUMSTATIN; VASCULOTROPIN A;

APOPTOSIS; DIABETIC NEPHROPATHY; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; GLOMERULOSCLEROSIS; HUMAN; HYPERGLYCEMIA; HYPERINSULINEMIA; INSULIN RESISTANCE; INSULIN SENSITIVITY; KIDNEY HYPERTROPHY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEINURIA; REVIEW; SIGNAL TRANSDUCTION;

ANGIOPOIETINS; DIABETIC NEPHROPATHY (DN); DIPEPTIDYL PEPTIDASE-4 (DPP-4) INHIBITORS; ENDOSTATIN; GLUCAGON LIKE PEPTIDE-1 (GLP-1); INSULIN; INSULIN RECEPTOR SUBSTRATE 1 (IRS1); PROTEIN KINASE C (PKC); SRC HOMOLOGY-2 DOMAIN CONTAINING PHOSPHATASE-1 (SHP-1); TUMSTATIN; VASCULAR ENDOTHELIAL GROWTH FACTOR (VEGF);

ANIMALS; CYTOPROTECTION; DIABETIC NEPHROPATHIES; DIPEPTIDYL-PEPTIDASE IV INHIBITORS; GLUCAGON-LIKE PEPTIDE 1; HEME OXYGENASE-1; HUMANS; HYPOGLYCEMIC AGENTS; INSULIN; KIDNEY; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84883808369     PISSN: 10568727     EISSN: 1873460X     Source Type: Journal    
DOI: 10.1016/j.jdiacomp.2013.03.003     Document Type: Review

References (68)

1. T. Alon, I. Hemo, A. Itin, J. Pe'er, J. Stone, and E. Keshet Vascular endothelial growth factor acts as a survival factor for newly formed retinal vessels and has implications for retinopathy of prematurity Nat Med 1 1995 1024 1028
2. F. Bock, K. Shahzad, H. Wang, S. Stoyanov, J. Wolter, and W. Dong Activated protein C ameliorates diabetic nephropathy by epigenetically inhibiting the redox enzyme p66Shc Proc Natl Acad Sci U S A 110 2013 648 653
3. B.M. Brenner, M.E. Cooper, D. de Zeeuw, W.F. Keane, W.E. Mitch, and H.H. Parving Effects of losartan on renal and cardiovascular outcomes in patients with type 2 diabetes and nephropathy N Engl J Med 345 2001 861 869
4. B.P. Bullock, R.S. Heller, and J.F. Habener Tissue distribution of messenger ribonucleic acid encoding the rat glucagon-like peptide-1 receptor Endocrinology 137 1996 2968 2978
5. P. Carmeliet, V. Ferreira, G. Breier, S. Pollefeyt, L. Kieckens, and M. Gertsenstein Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele Nature 380 1996 435 439
6. S. Chen, and F.N. Ziyadeh Vascular endothelial growth factor and diabetic nephropathy Curr Diab Rep 8 2008 470 476
7. S.G. Chrysant, and G.S. Chrysant Clinical implications of cardiovascular preventing pleiotropic effects of dipeptidyl peptidase-4 inhibitors Am J Cardiol 109 2012 1681 1685
8. K. Cusi, K. Maezono, A. Osman, M. Pendergrass, M.E. Patti, and T. Pratipanawatr Insulin resistance differentially affects the PI 3-kinase- and MAP kinase-mediated signaling in human muscle J Clin Invest 105 2000 311 320
9. D.J. Drucker The biology of incretin hormones Cell Metab 3 2006 153 165
10. A.A. Elmarakby, J. Faulkner, B. Baban, M.A. Saleh, and J.C. Sullivan Induction of hemeoxygenase-1 reduces glomerular injury and apoptosis in diabetic spontaneously hypertensive rats Am J Physiol Renal Physiol 302 2012 F791 800
11. O. Erdogdu, D. Nathanson, A. Sjoholm, T. Nystrom, and Q. Zhang Exendin-4 stimulates proliferation of human coronary artery endothelial cells through eNOS-, PKA- and PI3K/Akt-dependent pathways and requires GLP-1 receptor Mol Cell Endocrinol 325 2010 26 35
12. V. Eremina, J.A. Jefferson, J. Kowalewska, H. Hochster, M. Haas, and J. Weisstuch VEGF inhibition and renal thrombotic microangiopathy N Eng J Med 358 2008 1129 1136
13. V. Eremina, M. Sood, J. Haigh, A. Nagy, G. Lajoie, and N. Ferrara Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases J Clin Invest 111 2003 707 716
14. M. Federici, A. Pandolfi, E.A. De Filippis, G. Pellegrini, R. Menghini, and D. Lauro G972R IRS-1 variant impairs insulin regulation of endothelial nitric oxide synthase in cultured human endothelial cells Circulation 109 2004 399 405
15. N. Ferrara Vascular endothelial growth factor: Basic science and clinical progress Endocr Rev 25 2004 581 611
16. N. Ferrara, and H.P. Gerber The role of vascular endothelial growth factor in angiogenesis Acta Haematol 106 2001 148 156
17. Y. Fujio, and K. Walsh Akt mediates cytoprotection of endothelial cells by vascular endothelial growth factor in an anchorage-dependent manner J Biol Chem 274 1999 16349 16354
18. C.A. Fulcher, J.E. Gardiner, J.H. Griffin, and T.S. Zimmerman Proteolytic inactivation of human factor VIII procoagulant protein by activated human protein C and its analogy with factor V Blood 63 1984 486 489
19. P. Geraldes, K. Yagi, Y. Ohshiro, Z. He, Y. Maeno, and J. Yamamoto-Hiraoka Selective regulation of heme oxygenase-1 expression and function by insulin through IRS1/phosphoinositide 3-kinase/Akt-2 pathway J Biol Chem 283 2008 34327 34336
20. H.P. Gerber, V. Dixit, and N. Ferrara Vascular endothelial growth factor induces expression of the antiapoptotic proteins Bcl-2 and A1 in vascular endothelial cells J Biol Chem 273 1998 13313 13316
21. H.P. Gerber, K.J. Hillan, A.M. Ryan, J. Kowalski, G.A. Keller, and L. Rangell VEGF is required for growth and survival in neonatal mice Development 126 1999 1149 1159
22. H.P. Gerber, A. McMurtrey, J. Kowalski, M. Yan, B.A. Keyt, and V. Dixit Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3'-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation J Biol Chem 273 1998 30336 30343
23. P. Gil-Bernabe, C.N. D'Alessandro-Gabazza, M. Toda, D. Boveda Ruiz, Y. Miyake, and T. Suzuki Exogenous activated protein C inhibits the progression of diabetic nephropathy J Thromb Haemost 10 2012 337 346
24. A. Gruber, E. Mori, G.J. del Zoppo, L. Waxman, and J.H. Griffin Alteration of fibrin network by activated protein C Blood 83 1994 2541 2548
25. C.E. Hafer-Macko, F.M. Ivey, K.A. Gyure, J.D. Sorkin, and R.F. Macko Thrombomodulin deficiency in human diabetic nerve microvasculature Diabetes 51 2002 1957 1963
26. Z. He, D.M. Opland, K.J. Way, K. Ueki, N. Bodyak, and P.M. Kang Regulation of vascular endothelial growth factor expression and vascularization in the myocardium by insulin receptor and PI3K/Akt pathways in insulin resistance and ischemia Arterioscler Thromb Vasc Biol 26 2006 787 793
27. K. Ichinose, Y. Maeshima, Y. Yamamoto, M. Kinomura, K. Hirokoshi, and H. Kitayama 2-(8-hydroxy-6-methoxy-1-oxo-1 h-2-benzopyran-3-yl) propionic acid, an inhibitor of angiogenesis, ameliorates renal alterations in obese type 2 diabetic mice Diabetes 55 2006 1232 1242
28. K. Ichinose, Y. Maeshima, Y. Yamamoto, H. Kitayama, Y. Takazawa, and K. Hirokoshi Antiangiogenic endostatin peptide ameliorates renal alterations in the early stage of a type 1 diabetic nephropathy model Diabetes 54 2005 2891 2903
29. B. Isermann, I.A. Vinnikov, T. Madhusudhan, S. Herzog, M. Kashif, and J. Blautzik Activated protein C protects against diabetic nephropathy by inhibiting endothelial and podocyte apoptosis Nat Med 13 2007 1349 1358
30. Z.Y. Jiang, Y.W. Lin, A. Clemont, E.P. Feener, K.D. Hein, and M. Igarashi Characterization of selective resistance to insulin signaling in the vasculature of obese Zucker (fa/fa) rats J Clin Invest 104 1999 447 457
31. J.E. Kim, S.E. Song, Y.W. Kim, J.Y. Kim, S.C. Park, and Y.K. Park Adiponectin inhibits palmitate-induced apoptosis through suppression of reactive oxygen species in endothelial cells: involvement of cAMP/protein kinase A and AMP-activated protein kinase Journal of Endocrinology 207 1 2010 35 44
32. R. Kodera, K. Shikata, H.U. Kataoka, T. Takatsuka, S. Miyamoto, and M. Sasaki Glucagon-like peptide-1 receptor agonist ameliorates renal injury through its anti-inflammatory action without lowering blood glucose level in a rat model of type 1 diabetes Diabetologia 54 2011 965 978
33. C.H. Ku, K.E. White, A. Dei Cas, A. Hayward, Z. Webster, and R. Bilous Inducible overexpression of sFlt-1 in podocytes ameliorates glomerulopathy in diabetic mice Diabetes 57 2008 2824 2833
34. K. Kuboki, Z.Y. Jiang, N. Takahara, S.W. Ha, M. Igarashi, and T. Yamauchi Regulation of endothelial constitutive nitric oxide synthase gene expression in endothelial cells and in vivo: A specific vascular action of insulin Circulation 101 2000 676 681
35. M.E. Lee, M.S. Dhadly, D.H. Temizer, J.A. Clifford, M. Yoshizumi, and T. Quertermous Regulation of endothelin-1 gene expression by Fos and Jun J Biol Chem 266 1991 19034 19039
36. S.C. Lee, S.H. Han, J.J. Li, S.H. Lee, D.S. Jung, and S.J. Kwak Induction of heme oxygenase-1 protects against podocyte apoptosis under diabetic conditions Kidney Int 76 2009 838 848
37. S. Lee, W. Kim, S.O. Moon, M.J. Sung, D.H. Kim, and K.P. Kang Renoprotective effect of COMP-angiopoietin-1 in db/db mice with type 2 diabetes Nephrol Dial Transplant 22 2007 396 408
38. E.J. Lewis, L.G. Hunsicker, W.R. Clarke, T. Berl, M.A. Pohl, and J.B. Lewis Renoprotective effect of the angiotensin-receptor antagonist irbesartan in patients with nephropathy due to type 2 diabetes N Engl J Med 345 2001 851 860
39. H. Liu, A.E. Dear, L.B. Knudsen, and R.W. Simpson A long-acting glucagon-like peptide-1 analogue attenuates induction of plasminogen activator inhibitor type-1 and vascular adhesion molecules J Endocrinol 201 2009 59 66
40. W.J. Liu, S.H. Xie, Y.N. Liu, W. Kim, H.Y. Jin, and S.K. Park Dipeptidyl peptidase IV inhibitor attenuates kidney injury in streptozotocin-induced diabetic rats J Pharmacol Exp Ther 340 2012 248 255
41. A. Mima, J. Hiraoka-Yamomoto, Q. Li, M. Kitada, C. Li, and P. Geraldes Protective effects of GLP-1 on glomerular endothelium and its inhibition by PKCbeta activation in diabetes Diabetes 61 2012 2967 2979
42. A. Mima, M. Kitada, P. Geraldes, Q. Li, M. Matsumoto, and K. Mizutani Glomerular VEGF resistance induced by PKCdelta/SHP-1 activation and contribution to diabetic nephropathy FASEB J 26 2012 2963 2974
43. A. Mima, Y. Ohshiro, M. Kitada, M. Matsumoto, P. Geraldes, and C. Li Glomerular-specific protein kinase C-β-induced insulin receptor substrate-1 dysfunction and insulin resistance in rat models of diabetes and obesity Kidney International 79 8 2011 883 896
44. M. Montagnani, H. Chen, V.A. Barr, and M.J. Quon Insulin-stimulated activation of eNOS is independent of Ca2 + but requires phosphorylation by Akt at Ser(1179) J Biol Chem 276 2001 30392 30398
45. E.D. Motley, S.M. Kabir, C.D. Gardner, K. Eguchi, G.D. Frank, and T. Kuroki Lysophosphatidylcholine inhibits insulin-induced Akt activation through protein kinase C-alpha in vascular smooth muscle cells Hypertension 39 2002 508 512
46. S. Nakamaki, H. Satoh, A. Kudoh, Y. Hayashi, H. Hirai, and T. Watanabe Adiponectin reduces proteinuria in streptozotocin-induced diabetic Wistar rats Exp Biol Med 236 2011 614 620
47. K. Naruse, C. Rask-Madsen, N. Takahara, S.W. Ha, K. Suzuma, and K.J. Way Activation of vascular protein kinase C-beta inhibits Akt-dependent endothelial nitric oxide synthase function in obesity-associated insulin resistance Diabetes 55 2006 691 698
48. R.F. Nicosia, S.V. Nicosia, and M. Smith Vascular endothelial growth factor, platelet-derived growth factor, and insulin-like growth factor-1 promote rat aortic angiogenesis in vitro Am J Pathol 145 1994 1023 1029
49. L.A. Nikolaidis, S. Mankad, G.G. Sokos, G. Miske, A. Shah, and D. Elahi Effects of glucagon-like peptide-1 in patients with acute myocardial infarction and left ventricular dysfunction after successful reperfusion Circulation 109 2004 962 965
50. T. Nystrom, M.K. Gutniak, Q. Zhang, F. Zhang, J.J. Holst, and B. Ahren Effects of glucagon-like peptide-1 on endothelial function in type 2 diabetes patients with stable coronary artery disease Am J Physiol Endocrinol Metab 287 2004 E1209 1215
51. F.J. Oliver, G. de la Rubia, E.P. Feener, M.E. Lee, M.R. Loeken, and T. Shiba Stimulation of endothelin-1 gene expression by insulin in endothelial cells J Biol Chem 266 1991 23251 23256
52. N. Ouchi, S. Kihara, Y. Arita, Y. Okamoto, K. Maeda, and H. Kuriyama Adiponectin, an adipocyte-derived plasma protein, inhibits endothelial NF-kappaB signaling through a cAMP-dependent pathway Circulation 102 2000 1296 1301
53. R. Ouedraogo, X. Wu, S.Q. Xu, L. Fuchsel, H. Motoshima, and K. Mahadev Adiponectin suppression of high-glucose-induced reactive oxygen species in vascular endothelial cells: evidence for involvement of a cAMP signaling pathway Diabetes 55 6 2006 1840 1846
54. E.O. Ptilovanciv, G.S. Fernandes, L.C. Teixeira, L.A. Reis, E.A. Pessoa, and M.B. Convento Heme oxygenase 1 improves glucoses metabolism and kidney histological alterations in diabetic rats Diabetol Metab Syndr 5 2013 3
55. C. Rask-Madsen, E. Buonomo, Q. Li, K. Park, A.C. Clermont, and O. Yerokun Hyperinsulinemia does not change atherosclerosis development in apolipoprotein E null mice Arterioscler Thromb Vasc Biol 32 2012 1124 1131
56. C. Rask-Madsen, and G.L. King Mechanisms of disease: Endothelial dysfunction in insulin resistance and diabetes Nat Clin Pract Endocrinol Metab 3 2007 46 56
57. C. Rask-Madsen, Q. Li, B. Freund, D. Feather, R. Abramov, and I.H. Wu Loss of insulin signaling in vascular endothelial cells accelerates atherosclerosis in apolipoprotein E null mice Cell Metab 11 2010 379 389
58. B.F. Schrijvers, A.S. De Vriese, R.G. Tilton, J. Van de Voorde, L. Denner, and N.H. Lameire Inhibition of vascular endothelial growth factor (VEGF) does not affect early renal changes in a rat model of lean type 2 diabetes Horm Metab Res 37 2005 21 25
59. M.P. Seldon, G. Silva, N. Pejanovic, R. Larsen, I.P. Gregoire, and J. Filipe Heme oxygenase-1 inhibits the expression of adhesion molecules associated with endothelial cell activation via inhibition of NF-kappaB RelA phosphorylation at serine 276 J Immunol 179 2007 7840 7851
60. K. Sison, V. Eremina, H. Baelde, W. Min, M. Hirashima, and I.G. Fantus Glomerular structure and function require paracrine, not autocrine, VEGF-VEGFR-2 signaling J Am Soc Nephrol 21 2010 1691 1701
61. S.H. Sung, F.N. Ziyadeh, A. Wang, P.E. Pyagay, Y.S. Kanwar, and S. Chen Blockade of vascular endothelial growth factor signaling ameliorates diabetic albuminuria in mice J Am Soc Nephrol 17 2006 3093 3104
62. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. The Diabetes Control and Complications Trial Research Group N Engl J Med 329 1993 977 986
63. G. Thurston, J.S. Rudge, E. Ioffe, H. Zhou, L. Ross, and S.D. Croll Angiopoietin-1 protects the adult vasculature against plasma leakage Nat Med 6 2000 460 463
64. M.J. Tracz, J.P. Juncos, J.P. Grande, A.J. Croatt, A.W. Ackerman, and Z.S. Katusic Induction of heme oxygenase-1 is a beneficial response in a murine model of venous thrombosis Am J Pathol 173 2008 1882 1890
65. J. Tran, Z. Master, J.L. Yu, J. Rak, D.J. Dumont, and R.S. Kerbel A role for survivin in chemoresistance of endothelial cells mediated by VEGF Proc Natl Acad Sci U S A 99 2002 4349 4354
66. Effect of intensive blood-glucose control with metformin on complications in overweight patients with type 2 diabetes (UKPDS 34). UK Prospective Diabetes Study (UKPDS) Group Lancet 352 1998 854 865
67. G.I. Welsh, L.J. Hale, V. Eremina, M. Jeansson, Y. Maezawa, and R. Lennon Insulin signaling to the glomerular podocyte is critical for normal kidney function Cell Metab 12 2010 329 340
68. Y. Yamamoto, Y. Maeshima, H. Kitayama, S. Kitamura, Y. Takazawa, and H. Sugiyama Tumstatin peptide, an inhibitor of angiogenesis, prevents glomerular hypertrophy in the early stage of diabetic nephropathy Diabetes 53 2004 1831 1840